Comparative analysis of genetic testing utilization rates among people with and without disabilities in South Korea from 2016 to 2019, focusing on malignant neoplasms: A national population‐based study

Abstract Introduction Oncogene testing is widely used to detect or direct cancer treatments. Compared to people without disabilities, people with disabilities in Korea have a lower cancer incidence rate but a fivefold higher cancer mortality rate, implying delayed detection. Methods We used an administrative database combining disability status and care utilization to analyze every case of cancer‐related genetic testing paid for by the National Health Insurance Services of Korea between 2016 and 2019. We first compared percentages of individuals who had taken a registered genetic test by their disability statuses. We then compared the most frequently utilized tests between individuals with and without disabilities. Results Korean citizens, 175,000 in total, underwent at least one of the 192 registered cancer‐related genetic tests between 2016 and 2019. People with disabilities utilized these genetic tests at higher rates than those without disabilities, regardless of sex or age. Among people aged ≥40 years, lung and colorectal cancer‐related tests were most frequently utilized, regardless of disability status. Conclusion Although the cancer‐related genetic test uptake rate is higher among people with disabilities than among those without disabilities, it is still possible that information on these tests is not as readily available to people with disabilities. Therefore, it is imperative for the government to actively devise strategies to enhance national cancer screening rates among people with disabilities.


| INTRODUCTION
Just 30 years ago, cancer resembled a death sentence. 1The fatality rate of cancer has considerably decreased in the search for a cure.However, several types of cancer remain fatal and are yet to be overcome by modern medicine.The risk of certain types of cancer is higher in modern times because of factors such as smoking, air and water pollution, and lifestyle changes. 2 The Korean National Health Insurance statistics confirm this trend.According to Statistics Korea, cancer was the leading cause of death in 2021 among Koreans (161.1/100,000persons), followed by heart disease (61.5/100,000 persons).These numbers differed by more than 2.5 times. 3According to the Korea Central Cancer Registry, the number of new patients with cancer in 2020 was 247,952, and the agestandardized cancer incidence has been steadily increasing since 2015. 47][8] In fact, cancer is the main cause of death in people with disabilities in Korea, who comprise a medically vulnerable group.The cancer mortality and prevalence rates among people with disabilities are 1.05 and 5.02 times higher, respectively, than those among people without disabilities, despite the incidence rate of people with disabilities being marginally lower, at 0.90 times that of people without disabilities. 9,10Similarly, people with severe disabilities (Grades 1-3) show higher mortality rates than those with mild disabilities (Grades 4-6), despite the incidence rate being marginally lower.
The National Health Insurance Service (NHIS) of Korea covered genetic testing, one of the advanced medical technologies related to cancer on a national scale in order to reduce the burden of cancer.This genetic testing includes various purposes such as cancer screening, diagnosis, and treatment.Since the genetic testing covered in health insurance is supported either fully or partially by the insurance for people with disabilities, it provides excellent medical support for them to lower the burden related to cancer.However, separate from medical expense support, the discussion on whether disabled individuals are actually utilizing cancer-related genetic testing through medical cost support services is distinct.
There are various types of genetic testing, including germline genetic testing, which can identify genetic mutations present in an individual is germ cells, and somatic genetic testing, which can identify genetic mutations present in non-germ cells.In this study, we referred to these types collectively as genetic testing.[13] Genetic testing detects specific harmful mutations in genes that increase the risk of developing cancer or informs genetic susceptibility to specific types of cancer that are hereditary.In addition to predicting the risk of cancer, tumor DNA sequencing can contribute to increasing the cancer survival rate by allowing customized treatment of the cancer cells according to gene changes of the said cancer cells.For example, of the three types of RAT Sarcoma virus (RAS), the oncogene Kirsten Rat Sarcoma Viral Oncogene Homolog (KRAS) is known to have a 40% mutation rate, whereas the Neuroblastoma Rat Sarcoma Viral Oncogene Homolog (NRAS) has a mutation rate of approximately 5%-8%. 14Medical teams can predict responsiveness to existing targeted therapies by verifying the presence or absence of these mutations.New therapies targeting these mutations are currently under development.
Research on whether individuals with disabilities are effectively utilizing high-utilization genetic testing like this has not been well conducted thus far.While there are several studies on cancer-related genetic-test utilization, disability status is rarely recognized as a factor, either as a motivator or a barrier.To the best of our knowledge, whether genetic-test utilization patterns differ by disability status is yet to be studied.
Therefore, in this study, we aimed to analyze the entire population using national data sources to identify which genetic tests are actually widely utilized by individuals with disabilities in Korea, as well as to assess the screening rates for cancer among this group.Based on our findings, we intend to propose social and institutional measures to improve earlier detection and better treatment for cancer for people with disabilities.

| Data sources and sample criteria
As the majority of Korean citizens are enrolled in medical insurance, we used a national administrative dataset, the National Health Insurance Service of Korea (NHIS) and Korean Statistical Information Service (KOSIS), which comprises the entire record of genetic tests utilized by Korean citizens.We also identified individuals with disabilities by their Ministry of Health and Welfare disability registration statuses, leaving little room for measurement error. 15Patients who underwent genetic testing between 2016 and 2019 were included in this study.The NHIS database stores the premier data of Korea, and includes information on health insurance qualifications, insurance premiums, diagnoses, and procedure codes of care paid by the national health insurance.We included individuals with Korean citizenship who underwent one of the 192 genetic tests (Appendix) listed in the National Health Insurance Payment Scheme after approval by the National Evidence-based Healthcare Collaborating Agency of Korea through their New Medical Technology Evaluation.The total number of patients who underwent genetic testing between 2016 and 2019 was 175,330.We studied the annual trends, demographic characteristics, and medical care utilization of these individuals based on their disability status.
Types of genetic tests mainly include those used for various purposes, such as preventing specific rare diseases or diagnosing and treating cancer.The following genetic tests are the main genetic tests in the top five shown in the results of this study.

| Ethical considerations
This study complied with the Guidelines on De-Identification of Personal Data of Korea and was approved by the Institutional Review Board of Kyung Hee University [IRB No. KHSIRB-20-074(EA)] as a review exemption.
Given that the study used de-identified data, the board waived the requirement for obtaining informed consent from the participants.

| Descriptive statistics
The

| Status of genetic testing use according to disability type
The analysis included 15 legally defined types of disabilities in Korea.Every year, an increasing number of people with disabilities undergo genetic testing.In 2016, when genetic testing was registered as a reimbursement, it was 0.16%, but in 2019, it approximately doubled to 0.27%.In particular, the usage rate of people with internal organ disabilities was the highest at 0.48%, and the usage rate of people with mental disabilities was the lowest at 0.09%.We could not analyze detailed test types by disability type to prevent personal identification because of the small number of users (Table 2).
3.3 | Differences in the percentage of patients using genetic testing according to disability status A higher proportion of people with disabilities utilized genetic testing than those without disabilities (p < 0.001), regardless of sex and age (Table 3).This difference grows every year.4).

| Cancer screening rates for people with disabilities by cancer type
In individuals with disabilities, the rate of cancer screening was generally low for all types except lung cancer.When considering specific types, excluding cervical cancer, which was only screened in women, lung and colon cancers had the lowest screening rates.There was a notable trend: younger individuals, those with lower income, more severe disabilities, or a shorter duration since disability registration tended to have lower cancer screening rates.Particularly, people with mental disabilities recorded the lowest screening rates.Individuals with internal organ disabilities followed the low screening rates, and then those with disabilities affecting major external body functions (Table 5) (Figure 1).

| DISCUSSION
This study aims to achieve two objectives.First, it seeks to determine the frequency and types of genetic tests utilized by individuals with disabilities, specifically focusing on identifying the types of cancer that are most needed among this population.Second, it aims to evaluate the cancer screening rates among individuals with disabilities for the specific types of cancer identified earlier.
The results of the first objective are as follows.The inclusion of genetic tests in the National Health Insurance Service is increasing, leading to a rise in the frequency of genetic testing.The study findings revealed that the national health insurance expenditure on genetic testing amounted to 6.2 billion in 2016, 9.8 billion in 2017, and approximately 11.8 billion in 2018.
In Korea, the government continues to supplement the list of genetic tests on national health insurance benefits to meet the public demand for healthcare and promote general health.Although numerous citizens benefit from these tests, people with disabilities might not benefit as much because of difficulties in accessing and understanding emerging medical technologies. 16A B L E 3 Comparison of the proportions of patients who utilize oncogene genetic tests for persons with and without disabilities (unit: %).

2017
The Boldface is intended to distinguish between each type of disability.
People with disabilities aged <40 years primarily undergo tests for genetic diseases, such as lymphoproliferative diseases, acute myelocytic leukemia, and chronic myeloproliferative diseases.Among those aged ≥40 years, who accounted for 88.4% of the total number of people with disabilities, the top three most frequently used tests were colorectal and lung cancer-related (KRAS, NRAS, and EGFR).
Cancer is the most common cause of death for people with disabilities in Korea.The crude death rate for the entire population because of cancer is 161.1/100,000people, whereas the number for people with disabilities is 3.8 times higher at 604.3/100,000 people.In other words, cancer is more lethal in individuals with disabilities than in those without. 9This result is consistent with findings in studies conducted in other countries. 6,17Our findings show that among people with disabilities aged 40 years and older, genetic tests related to colorectal and lung cancer are the most frequently used.These numbers imply a critical need to mitigate cancer risk in individuals with disabilities at various stages, including prevention, diagnosis, treatment, and care.
Based on these findings, we analyzed the cancer screening rates among individuals with disabilities focusing on two specific types of cancer selected from among numerous cancers: lung cancer and colorectal cancer.
As of 2020, the cancer screening rate among people with disabilities was 39.2%, which was lower than the cancer screening rate of 55.3% among people without disabilities in South Korea. 18Among different types of disabilities, people with brain lesions, intellectual disabilities, and those on the autism spectrum have lower cancer screening rates. 19egarding cancer type, the colorectal cancer screening rate through methods such as colonoscopy or fecal occult blood testing was 30.3% for people with disabilities and 35.2% for people without disabilities, both of which are lower than all averages for cancer screening rates. 20The percentages of lung cancer were 34.0% and 34.4% for people with and without disabilities, respectively, and a similar trend can also be found in studies conducted in other countries. 21he Korean government introduced the National Cancer Screening Program in 2002 to select six types of cancer to reduce cancer mortality through early cancer detection because of this risk. 22Among them, colon cancer and lung cancer are also included.However, the risk of cancer remains high among people with disabilities.One of the reasons for this is the lower uptake rate for cancer screening by people with disabilities due to multiple barriers. 23,24or example, in colonoscopy, which is mainly used in colon cancer screening, people with disabilities face barriers such as limitations in changing positions, difficulties in communication, lack of mobility equipment, etc.

T A B L E 4 (Continued)
T A B L E 5 Cancer screening rates for people with disabilities by cancer type.6][27][28] However, governmental institutional support in addressing these challenges remains notably insufficient.

General health checkup
It is crucial to improve early detection methods that are specifically designed for this population to reduce cancer-related risks among individuals with disabilities.Particularly, those with reduced cognitive abilities, such as individuals with brain lesions or those on the autism spectrum, could significantly benefit from specially tailored promotional efforts.These efforts might involve providing information in language formats that align with their cognitive understanding levels.For example, we can proactively identify and engage with high-risk groups within the disabled population, especially those with a familial history of cancer.We can foster greater awareness and participation by offering them comprehensive information about the advantages of early screening and genetic testing.
Additionally, the development and implementation of health literacy programs are vital.These programs should aim to demystify complex medical concepts, presenting them in a straightforward and accessible manner.Emphasizing the workings, benefits, and role of genetic testing in early cancer detection in an easily comprehensible language can further promote screening uptake.

| LIMITATIONS
In Korea, individuals with disabilities are often overlooked in medical research and healthcare policy debates. 29Specifically, research focusing on genetic testing for people with disabilities has been notably absent, only garnering attention recently.While genetic testing holds significant relevance for this demographic, it presents various challenges that must be addressed.
Although this study offers valuable insights, it has certain limitations.The primary constraint is that the findings, although obtained from the National Health Insurance Service (NHIS) data in the Republic of Korea, are based on a relatively small sample of individuals with disabilities.Consequently, these results may not be widely generalizable.Second, the low number of participants who underwent genetic testing, relative to the diversity of tests available, limited the depth of our analysis.Detailed analysis was further constrained to avoid the risk of individual identification.Despite these limitations, the study is noteworthy as it pioneers the exploration of genetic testing needs among people with disabilities in Korea.Additionally, the results are discussed in the context of Korea's current health and welfare policies.Further *The examination rate was calculated based on the number of people subject to examination/number of people examined.TABLE 5 (Continued)  research, incorporating data from other countries, is essential to enhance understanding and substantiate our findings.

| CONCLUSION
This study represents a pioneering analysis of the utilization of genetic testing among individuals with disabilities in Korea, identifying the specific diseases for which such testing is most commonly employed in this group.As far as we are aware, this marks the first study in South Korea to explore the rate of genetic testing for cancer using national data among people with disabilities.
Our research made significant findings using data from the National Health Insurance database and supplemented by other reliable sources like Statistical Korea and the National Office of Statistics.Notably, the most crucial genetic tests for people with disabilities were those related to lung and colon cancer.However, despite the heightened need and risk in this demographic, the rate of testing for lung and colon cancer through national health checkups was lower compared to other cancer types.This disparity suggests potential missed opportunities for early cancer detection in older adults with disabilities.Therefore, it is imperative for the government to actively devise strategies to enhance national cancer screening rates among people with disabilities.Such measures could pave the way for people with disabilities to lead lives of equitable health and well-being.

ETHICAL APPROVAL AND PATIENT CONSENT
This study complied with the Guidelines on De-Identification of Personal Data of Korea and was approved by the Institutional Review Board of Kyung Hee University [IRB No. KHSIRB-20-074(EA)] as a review exemption.Given that the study used de-identified data, the board waived the requirement for obtaining informed consent from the participants.
F I G U R E 1 Cancer screening rates for people with disabilities by cancer type (%).
data were prepared as of 2020 because the country has not yet provided the data for 2021.
number of genetic tests registered in the National Health Insurance payment scheme gradually increased from 92 in 2016 to 181 in 2017 and 192 in 2018.Accordingly, the frequency of genetic testing also increased from 38,239 in 2016 to 56,883 in 2017 and 70,396 in 2018.The number of patients who underwent genetic testing increased from 28,924 in 2016 to 56,118 in 2019.Reflecting these upward trends, the cost of genetic testing claims paid by national health insurance increased from approximately 6.2 billion in 2016 to 9.8 billion in 2017 and 11.8 billion in 2018 (Table 1).
T A B L E 2 Status of genetic testing according to disability type (Unit: persons).

proportion of patients who utilized oncogene genetic tests (%) p-value The proportion of patients who utilized oncogene genetic tests (%) p-value All People without disabilities People with disabilities All People without disabilities
Note: Numbers calculated by the authors based on the Population and Housing Census by Statistics Korea and Health Statistics of the People with Disabilities by the Ministry of Health and Welfare of Korea; p-values are for t-tests for differences between two proportions among people with and without disabilities.

2018 2019 The proportion of patients who utilized oncogene genetic tests (%) p-value The proportion of patients who utilized oncogene genetic tests (%) p-value All People without disabilities
*Include warfarin, phenytoin, fluoxetine, sertraline, and losartan.